C3

The life cycle of the deep-sea Bathymodiolus metaorganism: symbiont transmission and colonization of the host gill epithelium

Chemosynthetic symbioses evolved independently multiple times in at least nine animal phyla and from at least 12 lineages of free-living bacteria. They were first discovered at hydrothermal vents in the deep sea, and are also widespread in shallow marine habitats. Bathymodiolus mussels are one of the most abundant members of biological communities at marine hydrothermal vents and cold seeps. These hosts rely on a dense community of intracellular symbiotic bacteria in their gill epithelia that use reduced chemicals from the environment such as hydrogen sulfide and methane as an energy source to fix carbon dioxide or methane into biomass, which they pass on to feed their hosts. Bathymodiolus mussels are ideal for investigating the function and life history of symbiotic associations due to the relative simplicity of their symbiont community. Many Bathymodiolus species host two co-occurring symbionts, a single sulfur-oxidizing species and a single methane-oxidizing species. However, recent molecular studies and our preliminary metagenomic results have revealed that strain diversity within these two symbiont species is greater than previously assumed based on 16S rRNA gene analyses. Here we propose to investigate this symbiont strain diversity and its effects on metaorganism function, development and evolution. Our investigation will include the study of strain distribution within the gill tissue of individual mussels (Sub-project 1) and the characterization of symbiont population structure across multiple individual mussels (Sub-project 2). In our first sub-project, we will examine the strain diversity within individual mussels to better understand how these differ in their genomic and transcriptomic content, and thus function within the metaorganism using state-of-the art genomic technologies including single-cell genomics and a new method called Hi-C metagenomics. With these techniques we will be able to link distinct symbiont strains with mobile genetic elements such as phages and insertion sequences, which will provide insights into how these strains evolved. With in situ imaging, we plan to analyze the distribution patterns of distinct strains across an ontogenetic gradient within the host gill tissue, which will help to understand how the gill epithelium is colonized by symbionts throughout its lifetime. In our second sub-project, we will investigate genomic diversity and evolution at the symbiont population level using high-resolution metagenomics. This in-depth metagenomic data will allow us to tease apart the effects of symbiont transmission mode, colonization history over the lifetime of the mussel, and symbiont diversification within a host individual, which together are the main factors driving symbiont community diversity in all host-microbe associations. With high-resolution metagenomes, we will investigate the selective forces acting on symbiont genomes by quantifying ratios of non-synonymous to synonymous substitutions. This analysis will help to reveal the genomic mechanisms of symbiont adaptation to a host-associated lifestyle. Our research will lead to new insights into the ecology and evolutionary dynamics of symbiont acquisition and transmission mode, as well as a better understanding of the role of symbiont diversity in the ecology and evolution of metaorganisms.

Researchers

Dr. Anne Kupczok

Postdoctoral Researcher, Associated Junior Researcher
Kiel University Institute for General Microbiology

Rebecca Ansorge

PhD Candidate, Associated Junior Researcher
Max-Planck-Institute for Marine Microbiology

Publications

2017

Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction.

Popa O, Landan G, Dagan T (2017); ISME J., 11(2):543-554. doi: 10.1038/ismej.2016.116

Radiofrequency catheter ablation of atrioventricular node reentrant tachycardia in children with limited fluoroscopy.

Swissa M, Birk E, Dagan T, Naimer S A, Fogelman M, Einbinder T, Bruckheimer E, Fogelman R (2017); Int J Cardiol., pii:S0167-5273(16)34000-1. doi: 10.1016/j.ijcard.2017.01.128

Evolution of Chaperonin Gene Duplication in Stigonematalean Cyanobacteria (Subsection V).

Weissenbach J, Ilhan J, Bogumil D, Hülter N, Stucken K, Dagan T (2017); Genome Biol Evol., pii:evw287. doi: 10.1093/gbe/evw287

2016

Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis.

Ponnudurai R, Kleiner M, Sayavedra L, Petersen J M, Moche M, Otto A, Becher D, Takeuchi T, Satoh N, Dubilier N, Schweder T, Markert S (2016); ISME J., doi: 10.1038/ismej.2016.124

Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti.

Tavormina P L, Kellermann M Y, Antony C P, Tocheva E, Dalleska N, Jensen A J, Valentine D L, Hinrichs K U, Jensen G, Dubilier N, Orphan V J (2016); .Mol Microbiol., doi: 10.1111/mmi.13553

Marine genomics: News and views.

Ribeiro  M, Foote A D, Kupczok A, Frazão B, Limborg M T, Piñeiro R, Abalde S, Rocha S, da Fonseca R R (2016); Mar Genomics., pii: S1874-7787(16)30092-7. doi: 10.1016/j.margen.2016.09.002

Biophysical and Population Genetic Models Predict the Presence of “Phantom” Stepping Stones Connecting Mid-Atlantic Ridge Vent Ecosystems.

Breusing C, Biastoch A, Drews A, Metaxas A, Jollivet D, Vrijenhoek R C, Bayer T, Melzner F, Sayavedra L, Petersen J M, Dubilier N, Schilhabel M B, Rosenstiel P, Reusch T B (2016); Curr Biol., 26(17):2257-67. doi: 10.1016/j.cub.2016.06.062

A specific and widespread association between deep-sea Bathymodiolus mussels and a novel family of Epsilonproteobacteria.

Assié A, Borowski C, van der Heijden K, Raggi L, Geier B, Leisch N, Schimak M P, Dubilier N, Petersen J M (2016); Environ Microbiol Rep., doi: 10.1111/1758-2229.12442

Closely coupled evolutionary history of ecto- and endosymbionts from two distantly related animal phyla.

Zimmermann J, Wentrup C, Sadowski M, Blazejak A, Gruber-Vodicka H R, Kleiner M, Ott J A, Cronholm B, De Wit P, Erséus C, Dubilier N (2016); Mol Ecol., 25(13):3203-23. doi: 10.1111/mec.13554

DnaK-dependent accelerated evolutionary rate in prokaryotes.

Kadibelban A S, Bogumil D, Landan G, Dagan T (2016); Genome Biol Evol, 8(5):1590-9. doi: 10.1093/gbe/evw102.

2015

Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels.

Sayavedra L, Kleiner M, Ponnudurai R, Wetzel S, Pelletier E, Barbe V, Satoh N, Shoguchi E, Fink D, Breusing C, Reusch T B, Rosenstiel P, Schilhabel M B, Becher D, Schweder T, Markert S, Dubilier N, Petersen J M (2015); Elife, 4:e07966. doi:10.7554/eLife.07966

The Contribution of Genetic Recombination to CRISPR Array Evolution.

Kupczok A, Landan G, Dagan T (2015); Genome Biol Evol, 7(7):1925-39. doi: 10.1093/gbe/evv113

2014

Forever competent: Deep-sea bivalves are colonized by their chemosynthetic symbionts throughout their lifetime.

Wentrup C, Wendeberg A, Schimak M, Borowski C, Dubilier N (2014); Environ. Microbiol., 16:3699–3713. doi: 10.1111/1462-2920.12597

A SAGE based approach to human glomerular endothelium: defining the transcriptome, finding a novel molecule and highlighting endothelial diversity.

Sengoelge G, Winnicki W, Kupczok A, von Haeseler A, Schuster M, Pfaller W, Jennings P, Weltermann A, Blake S, Sunder-Plassmann G (2014); BMC Genomics., 15:725. doi: 10.1186/1471-2164-15-725

SMBE Satellite meeting on reticulated microbial evolution 2014–meeting report.

Dagan T, Bapteste E, McInerney J O, Martin W F (2014); Genome Biol Evol., 6(9):2206-9. doi: 10.1093/gbe/evu173

Motif depletion in bacteriophages infecting hosts with CRISPR systems.

Kupczok A, Bollback J P (2014); BMC Genomics., 15:663. doi: 10.1186/1471-2164-15-663

Integration of two ancestral chaperone systems into one: the evolution of eukaryotic molecular chaperones in light of eukaryogenesis.

Bogumil D, Alvarez-Ponce D, Landan G, McInerney J O, Dagan T (2014); Mol Biol Evol., 31(2):410-8. doi: 10.1093/molbev/mst212

2013

Metaproteomics reveals abundant transposase expression in mutualistic endosymbionts.

Kleiner M, Young J C, Shah M, VerBerkmoes N C, Dubilier N (2013), mBio; 4:3. doi: 10.1128/mBio.00223-13

Genomes of stigonematalean cyanobacteria (Subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids.

Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, Gould S B, Goremykin V V, Rippka R, Tandeau de Marsac N, Gugger M, Lockhart P J, Allen J F, Brune I, Maus I, Pühler A, Marti W (2013); Genome Biol Evol, 5:31-44. doi: 10.1093/gbe/evs117

Cyanobacterial defense mechanisms against foreign DNA transfer and their impact on genetic engineering.

Stucken K, Koch R, Dagan T (2013); Biol Res., 46(4):373-82. doi: 10.4067/S0716-97602013000400009

Complete Genome Sequence of the Novel Phage MG-B1 Infecting Bacillus weihenstephanensis.

Redondo R A, Kupczok A, Stift G, Bollback J P (2013); Genome Announc., 1(3). pii: e00216-13. doi: 10.1128/genomeA.00216-13

Probabilistic models for CRISPR spacer content evolution.

Kupczok A, Bollback J P (2013); BMC Evol Biol., 13:54. doi: 10.1186/1471-2148-13-54

Animals in a bacterial world, a new imperative for the life sciences.

McFall-Ngai M, Hadfield M, Bosch T C G, Carey H, Domazet-Loso T, Douglas A, Dubilier N, Eberl G, Fukami T, Gilbert S, Hentschel U, King N, Kjelleberg S, Knoll A, Kremer N, Mazmanian S, Metcalf J, Nealson K, Pierce N, Rawls J, Reid A, Ruby E, Rumpho M, Sanders J, Tautz D, Wernegreen J (2013); Proc Natl Acad Sci USA, 110(9):3229-36. doi: 10.1073/pnas.1218525110

2012

The cumulative impact of chaperone mediated folding on genome evolution.

Bogumil D, Dagan T (2012); Biochemistry, 51:9941-9953. doi: 10.1021/bi3013643

Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer.

Kleiner M, Petersen J M, Dubilier N (2012); Curr. Opin. Microbiol., 15:621-631. doi: 10.1016/j.mib.2012.09.003

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use.

Kleiner M, Wentrup C, Lott C, Teeling, H, Wetzel S, Young J, Chang Y-J, Shah M, VerBerkmoes NC, Zarzycki J, Fuchs G, Markert S, Hempel K, Voigt B, Becher D, Liebeke M, Lalk M, Albrecht D, Hecker M, Schweder T, Dubilier N (2012); Proc. Natl. Acad. Sci. USA., 109:E1173-E1182. doi: 10.1073/pnas.1121198109

Acquisition of a thousand eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea.

Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney J, Deppenmeier U, Martin W F (2012); Proc Natl Acad Sci USA, 109:20537-20542. doi: 10.1073/pnas.1209119109

Transformation and conjugal transfer of foreign genes into the filamentous multicellular cyanobacteria (subsection V) Fischerella and Chlorogloeopsis.

Stucken K, Ilhan J, Roettger M, Dagan T, Martin W F (2012); Curr Microbiol., 65(5):552-60. doi: 10.1007/s00284-012-0193-5

A consistent phylogenetic backbone for the fungi.

Ebersberger I, de Matos Simoes R, Kupczok A, Gube M, Kothe E, Voigt K, von Haeseler A (2012); Mol Biol Evol., 29(5):1319-34. doi: 10.1093/molbev/msr285

An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin.

Thiergart T, Landan G, Schenk M, Dagan T, Martin W F (2012); Genome Biol Evol., 4(4):466-85. doi: 10.1093/gbe/evs018

An exported chaperone system in P. falciparum infected erythrocytes.

Külzer S, Charnaud S, Riedel J, Mandal P, Dagan T, Crabb B S, Gilson P R, Przyborski J M (2012)

Trachipleistophora hominis prodives novel insights into reductive genome evolution in eukaryotes, in press.

Heinz E, Williams T, Nakjang S, Noël C J, Swan D C, Goldberg A V, Harris SR, Weinmaier T, Markert S, Becher D, Dagan T, Schweder T, Rattei T, Hall N, Hirt RP, Embley T M (2012)

Modern endosymbiotic theory: Getting lateral gene transfer into the equation.

Martin W F, Roettger M, Kloesges T, Thiergart T, Woehle C, Gould S, Dagan T (2012); J Endocytobiosis Cell Res, 23:1-5.

Gene transfers from organelles to the nucleus: How much, what happens, and why none in Elysia?

Martin W, Hazkani-Covo E, Shavit-Greivink L, Schmitt V, Händeler K, Gould S B, Landan G, Graur D, Dagan T (2012); Journal of Endocytobiosis and Cell Research, 23:16-20.

2011

A machine learning approach to identify hydrogenosomal proteins in Trichomonas vaginalis.

Burstein D, Gould S B, Zimorski V, Kloesges T, Kiosse F, Major P, Martin W F, Pupko T, Dagan T (2011)Eukaryot Cell., 11(2):217-28. doi: 10.1128/EC.05225-11

Trend and barriers to lateral gene transfer in prokaryotes.

Popa O, Dagan T (2011); Curr Opin Microbiol, 14(5):615-623. doi: 10.1016/j.mib.2011.07.027

Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia.

Woehle C, Dagan T, Martin W F, Gould S B (2011); Genome Biol Evol., 3:1220-30. doi: 10.1093/gbe/evr100

Hydrogen is an energy source for hydrothermal vent symbioses.

Petersen J M, Zielinski F U, Pape T, Seifert R, Moraru C, Amann R, Hourdez S, Girguis P R, Wankel S D, Barbe V, Pelletier E, Fink D, Borowski C, Bach W, Dubilier N (2011); Nature, 476:176-180. doi: 10.1038/nature10325

Split-based computation of majority-rule supertrees.

Kupczok A (2011); BMC Evol Biol., 11:205. doi: 10.1186/1471-2148-11-205

Networks uncover hidden lexical borrowing in Indo-European language evolution.

Shijulal N S, List J M, Geisler H, Fangerau H, Gray R D, Martin W, Dagan T (2011); Proc Biol Sci, 278:1794-803. doi: 10.1098/rspb.2010.1917

Directed networks reveal barriers and bypasses to lateral gene transfer in prokaryotes.

Popa O, Hazkani-Covo E, Landan G, Martin W, Dagan T (2011); Genome Res, 21(4):599-609. doi: 10.1101/gr.115592.110

Consequences of different null models on the tree shape bias of supertree methods.

Kupczok A (2011); Syst Biol., 60(2):218-25. doi: 10.1093/sysbio/syq086

Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths.

Kloesges T, Popa O, Martin W, Dagan T (2011); Mol Biol Evol., 28(2):1057-74. doi: 10.1093/molbev/msq297

Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plackobranchus ocellatus does not entail lateral transfer of algal nuclear genes.

Wagele H, Deusch O, Handeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould S B, Dagan T, Klussmann-Kolb A, Martin W (2011); Mol Biol Evol, 28(1):699-706. doi: 10.1093/molbev/msq239

2010

Accuracy of phylogeny reconstruction methods combining overlapping gene data sets.

Kupczok A, Schmidt H A, von Haeseler A (2010); Algorithms Mol Biol., 5:37. doi: 10.1186/1748-7188-5-37

Chaperonin-dependent accelerated substitution rates in prokaryotes.

Bogumil D, Dagan T (2010); Genome Biol Evol., 2010;2:602-8. doi: 10.1093/gbe/evq044

Evolution of spliceosomal introns following endosymbiotic gene transfer.

Ahmadinejad N, Dagan T, Gruenheit N, Martin W, Gabaldón T (2010); BMC Evol Biol., 10:57. doi: 10.1186/1471-2148-10-57

2009

Prokaryotic evolution and the tree of life are two different things.

Bapteste E, O’Malley M A, Beiko R G, Ereshefsky M, Gogarten J P, Franklin-Hall L, Lapointe F J, Dupré J, Dagan T, Boucher Y, Martin W (2009); Biol Direct, 4:34. doi: 10.1186/1745-6150-4-34

A machine-learning approach reveals that alignment properties alone can accurately predict inference of lateral gene transfer from discordant phylogenies.

Roettger M, Martin W, Dagan T (2009); Mol Biol Evol., 26(9):1931-9. doi: 10.1093/molbev/msp105

Getting a better picture of microbial evolution en route to a network of genomes.

Dagan T, Martin W (2009); Philos Trans R Soc Lond B Biol Sci., 364(1527):2187-96. doi: 10.1098/rstb.2009.0040

A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the alpha-proteobacterial mitochondrial ancestor.

Atteia A, Adrait A, Brugière S, Tardif M, van Lis R, Deusch O, Dagan T, Kuhn L, Gontero B, Martin W, Garin J, Joyard J, Rolland N (2009); Mol Biol Evol., 26(7):1533-48. doi: 10.1093/molbev/msp068

Microbiology. Seeing green and red in diatom genomes.

Dagan T, Martin W (2009); Science., 324(5935):1651-2. doi: 10.1126/science.1175765

Comment on ‘A congruence index for testing topological similarity between trees’.

Kupczok A, von Haeseler A (2009); Bioinformatics., 25(1):147-9. doi: 10.1093/bioinformatics/btn539

2008

Symbiotic diversity in marine animals: the art of harnessing chemosynthesis.

Dubilier N, Bergin C, Lott C (2008); Nature Reviews Microbiology, 6:725-740. doi: 10.1038/nrmicro1992

Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution.

Dagan T, Artzy-Randrup Y, Martin W (2008); Proc Natl Acad Sci USA, 105(29):10039–10044. doi: 10.1073/pnas.0800679105

An exact algorithm for the geodesic distance between phylogenetic trees.

Kupczok A, von Haeseler A, Klaere S (2008); J Comput Biol., 15(6):577-91. doi: 10.1089/cmb.2008.0068

Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor.

Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik K V, Allen J F, Martin W, Dagan T (2008); Mol Biol Evol., 25(4):748-61. doi: 10.1093/molbev/msn022

Evolutionary dynamics of introns in plastid-derived genes in plants: saturation nearly reached but slow intron gain continues.

Basu M K, Rogozin I B, Deusch O, Dagan T, Martin W, Koonin E V (2008); Mol Biol Evol., 25(1):111-9. doi: 10.1093/molbev/msm234

2007

Genome history in the symbiotic hybrid Euglena gracilis.

Ahmadinejad N, Dagan T, Martin W (2007); Gene., 402(1-2):35-9. doi: 10.1016/j.gene.2007.07.023

Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture.

Kilian B, Ozkan H, Walther A, Kohl J, Dagan T, Salamini F, Martin W (2007); Mol Biol Evol., 24(12):2657-68. doi: 10.1093/molbev/msm192

Diversity, relative abundance, and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico.

Duperron S, Sibuet M, MacGregor B J, Kuypers M M M, Fisher C R, Dubilier N (2007); Environ. Microbiol., 9(6):1423-1438. doi: 10.1111/j.1462-2920.2007.01259.x

Testing hypotheses without considering predictions.

Dagan T, Martin W (2007); Bioessays., 29(5):500-3. doi: 10.1002/bies.20566

The evolution of eukaryotes.

Martin W, Dagan T, Koonin E V, Dipippo J L, Gogarten J P, Lake J A (2007); Science., 316(5824):542-3. doi: 10.1126/science.316.5824.542c

The origin of mitochondria in light of a fluid prokaryotic chromosome model.

Esser C, Martin W, Dagan T (2007); Biol Lett., 3(2):180-4. doi: 10.1098/rsbl.2006.0582

Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution.

Dagan T, Martin W (2007); Proc Natl Acad Sci USA, 104(3):870–875. doi: 10.1073/pnas.0606318104

2006

Symbiosis insights through metagenomic analysis of a microbial consortium.

Woyke T, Teeling H, Ivanova N N, Richter M, Hunteman M, Gloeckner F O, Boffelli D, Barry KW, Shapiro H J, Mussmann M, Bergin C, Ruehland C, Amann R, Anderson I J, Szeto E, Kyrpides N C, Markowitz V M, Rubin E M, Dubilier N (2006); Nature, 443:950-955. doi: 10.1038/nature05192

Determinants of simulated RNA evolution.

Kupczok A, Dittrich P (2006); J Theor Biol., 238(3):726-35. doi: 10.1016/j.jtbi.2005.06.019

The “domino theory” of gene death: gradual and mass gene extinction events in three lineages of obligate symbiotic bacterial pathogens.

Dagan T, Blekhman R, Graur D (2006); Mol Biol Evol., 23(2):310-6. doi: 10.1093/molbev/msj036

2005

The comparative method rules! Codon volatility cannot detect positive Darwinian selection using a single genome sequence.

Dagan T, Graur D (2005); Mol Biol Evol., 22(3):496-500. doi: 10.1093/molbev/msi033

GC composition of the human genome: in search of isochores.

Cohen N, Dagan T, Stone L, Graur D (2005); Mol Biol Evol., 22(5):1260-72. doi: 10.1093/molbev/msi115

2004

Minimal conditions for exonization of intronic sequences: 5′ splice site formation in alu exons.

Sorek R, Lev-Maor G, Reznik M, Dagan T, Belinky F, Graur D, Ast G (2004);
Mol Cell., 14(2):221-31. doi: 10.1016/S1097-2765(04)00181-9

AluGene: a database of Alu elements incorporated within protein-coding genes.

Dagan T, Sorek R, Sharon E, Ast G, Graur D (2004); Nucleic Acids Res., 32:D489-92. doi: 10.1093/nar/gkh132

2003

pANT: a method for the pairwise assessment of nonfunctionalization times of processed pseudogenes.

Fleishman S J, Dagan T, Graur D (2003); Mol Biol Evol., 20(11):1876-80. doi: 10.1093/molbev/msg202

2002

Ratios of radical to conservative amino acid replacement are affected by mutational and compositional factors and may not be indicative of positive Darwinian selection.

Dagan T, Talmor Y, Graur D (2002); Mol Biol Evol., 19(7):1022-5. doi: 10.1093/oxfordjournals.molbev.a004161

2001

Endosymbiotic sulfate-reducing and sulfideoxidizing bacteria in a gutless marine worm (Oligochaeta, Annelida).

Dubilier N, Mülders C, Ferdelman T, de Beer D, Hentschke A, Klein M, Wagner M, Erséus C, Thiermann F, Krieger J, Giere O, Amann R (2001); Nature, 411:298-302. doi: 10.1038/35077067